Differential Impacts of the Head on Platynereis dumerilii Peripheral Circadian Rhythms

Abstract

The marine bristle worm Platynereis dumerilii is a useful functional model system for the study of the circadian clock and its interplay with others, e.g., circalunar clocks. The focus has so far been on the worm’s head. However, behavioral and physiological cycles in other animals typically arise from the coordination of circadian clocks located in the brain and in peripheral tissues. Here, we focus on peripheral circadian rhythms and clocks, revisit and expand classical circadian work on the worm’s chromatophores, investigate locomotion as read-out and include molecular analyses. We establish that different pieces of the trunk exhibit synchronized, robust oscillations of core circadian clock genes. These circadian core clock transcripts are under strong control of the light-dark cycle, quickly losing synchronized oscillation under constant darkness, irrespective of the absence or presence of heads. Different wavelengths are differently effective in controlling the peripheral molecular synchronization. We have previously shown that locomotor activity is under circadian clock control. Here, we show that upon decapitation worms exhibit strongly reduced activity levels. While still following the light-dark cycle, locomotor rhythmicity under constant darkness is less clear. We also observe the rhythmicity of pigments in the worm’s individual chromatophores, confirming their circadian pattern. These size changes continue under constant darkness, but cannot be re-entrained by light upon decapitation. Our works thus provides the first basic characterization of the peripheral circadian clock of P. dumerilii . In the absence of the head, light is essential as a major synchronization cue for peripheral molecular and locomotor circadian rhythms, while circadian changes in chromatophore size can continue for several days in the absence of light/dark changes and the head. Thus, in Platynereis the dependence on the head depends on the type of peripheral rhythm studied. These data show that peripheral circadian rhythms and clocks should also be considered in “non-conventional” molecular model systems, i.e., outside Drosophila melanogaster , Danio rerio , and Mus musculus , and build a basic foundation for future investigations of interactions of clocks with different period lengths in marine organisms.

Characterization of cephalic and non-cephalic sensory cell types provides insight into joint photo- and mechanoreceptor evolution

“…Since the expression levels of atp2b/c7424 in Platynereis TRE cells depend on r-opsin1 function, we wondered if they might also depend on illumination. Decapitated worm trunks are functionally relatively autonomous, maintain their ability to crawl and swim, aspects of their rhythmicity, and live for up to 2 weeks ( Figure 6B ; Arboleda et al, 2019 ). We cultured decapitated trunks of pMos{rops::egfp} vbci2 worms for 3–5 days in two distinct light conditions: (i) bright monochromatic blue light (~470 nm) and (ii) very dim white light ( Figure 6C ).…”

“…Video recording of worm behavior over several days was accomplished as described previously ( Arboleda et al, 2019 ; Veedin Rajan et al, 2021 ). Prior to recording, worms were incubated for 2–4 hr to allow them to build tubes, which is part of their normal behavior.…”

Exposure to Artificial Light at Night and the Consequences for Flora, Fauna, and Ecosystems

“…The data on invertebrates are not as abundant as for vertebrates, and relate mostly to insects, although more and more studies refer to marine invertebrates. All indicate that the clocks mediate the effects of photoperiod and temperature on a myriad of rhythmic daily and seasonal events ( Helfrich-Forster et al, 2011 ; Arboleda et al, 2019 ). The most obvious relate to feeding ( e. g., foraging in bees, and moths, bugs and mosquitoes bites), reproduction ( e.g ., courtship behaviour, mating and reproduction), and growth (larval and adult development, diapause, longevity) ( Helfrich-Forster et al, 2011 ; Bloch et al, 2013 ; Rougvie and O’Connor, 2013 ; Table 1 ).…”

Characterization of cephalic and non-cephalic sensory cell types provides insight into joint photo- and mechanoreceptor evolution

“…Video recording of worm behavior over several days was accomplished as described previously [59,63]. Prior to recording, worms were incubated for 2-4 hours to allow them to build tubes, which is part of their normal behavior.…”

“…Since the expression levels of atp2b/c7424 in Platynereis TREs depend on r-opsin1 function, we wondered if they might also depend on illumination.Decapitated worm trunks are functionally relatively autonomous, maintain their ability to crawl and swim, aspects of their rhythmicity and live for up to two weeks(Fig. 5B)[59]. We cultured decapitated trunks of pMos{rops::egfp} vbci2 worms for 3-5 days in two distinct light conditions: (i) bright monochromatic blue light (~470 nm); and (ii) very dim white light(Fig.…”